Localization of Motor Neurons and Central Pattern Generators for Motor Patterns Underlying Feeding Behavior in Drosophila Larvae

Motor systems can be functionally organized into effector organs (muscles and glands), the motor neurons, central pattern generators (CPG) and higher control centers of the brain. Using genetic and electrophysiological methods, we have begun to deconstruct the motor system driving Drosophila larval feeding behavior into its component parts. In this paper, we identify distinct clusters of motor neurons that execute head tilting, mouth hook movements, and pharyngeal pumping during larval feeding. This basic anatomical scaffold enabled the use of calcium-imaging to monitor the neural activity of motor neurons within the central nervous system (CNS) that drive food intake. Simultaneous nerve- and muscle-recordings demonstrate that the motor neurons innervate the cibarial dilator musculature (CDM) ipsi- and contra-laterally. By classical lesion experiments we localize a set of CPGs generating the neuronal pattern underlying feeding movements to the subesophageal zone (SEZ). Lesioning of higher brain centers decelerated all feeding-related motor patterns, whereas lesioning of ventral nerve cord (VNC) only affected the motor rhythm underlying pharyngeal pumping. These findings provide a basis for progressing upstream of the motor neurons to identify higher regulatory components of the feeding motor system.

[1]  W. O. Friesen,et al.  Neuronal control of leech swimming movements , 1989, Journal of Comparative Physiology A.

[2]  Donald M. Wilson.  The Central Nervous Control of Flight in a Locust , 1961 .

[3]  Simon G. Sprecher,et al.  The Serotonergic Central Nervous System of the Drosophila Larva: Anatomy and Behavioral Function , 2012, PloS one.

[4]  Ann-Shyn Chiang,et al.  Parallel Neural Pathways Mediate CO2 Avoidance Responses in Drosophila , 2013, Science.

[5]  E. Marder,et al.  Central pattern generators and the control of rhythmic movements , 2001, Current Biology.

[6]  W. Otto Friesen,et al.  Neuronal control of leech swimming movements , 1989, Journal of Comparative Physiology A.

[7]  J. C. Smith,et al.  Cellular Mechanisms Underlying Modulation of Breathing Pattern in Mammals a , 1989, Annals of the New York Academy of Sciences.

[8]  Stefan R. Pulver,et al.  Ultra-sensitive fluorescent proteins for imaging neuronal activity , 2013, Nature.

[9]  Ying Li,et al.  Serotonin Regulates Rhythmic Whisking , 2003, Neuron.

[10]  Stefan R. Pulver,et al.  Autonomous Circuitry for Substrate Exploration in Freely Moving Drosophila Larvae , 2012, Current Biology.

[11]  Richard Axel,et al.  A dimorphic pheromone circuit in Drosophila from sensory input to descending output , 2010, Nature.

[12]  R. M. Rose,et al.  Central generation of bursting in the feeding system of the snail, Lymnaea stagnalis. , 1979, The Journal of experimental biology.

[13]  C. Wu,et al.  Dual muscarinic and nicotinic action on a motor program in Drosophila. , 1991, Journal of neurobiology.

[14]  M. Sokolowski.  Drosophila larval foraging behavior: Digging , 1982, Animal Behaviour.

[15]  M. Goulding.  Circuits controlling vertebrate locomotion: moving in a new direction , 2009, Nature Reviews Neuroscience.

[16]  H. Heinzel,et al.  Anatomy of the stomatogastric nervous system associated with the foregut in Drosophila melanogaster and Calliphora vicina third instar larvae , 2008, Journal of morphology.

[17]  Elizabeth H. Chen,et al.  Antisocial, an intracellular adaptor protein, is required for myoblast fusion in Drosophila. , 2001, Developmental cell.

[18]  T. Wen,et al.  Developmental Control of Foraging and Social Behavior by the Drosophila Neuropeptide Y-like System , 2003, Neuron.

[19]  W. O. Friesen,et al.  Neuronal control of leech swimming. , 1995, Journal of neurobiology.

[20]  Julie H. Simpson,et al.  Mapping and manipulating neural circuits in the fly brain. , 2009, Advances in genetics.

[21]  S. Niederegger,et al.  From behavior to fictive feeding: anatomy, innervation and activation pattern of pharyngeal muscles of Calliphora vicina 3rd instar larvae. , 2009, Journal of insect physiology.

[22]  Sten Grillner,et al.  Biological Pattern Generation: The Cellular and Computational Logic of Networks in Motion , 2006, Neuron.

[23]  A. Selverston,et al.  Invertebrate central pattern generator circuits , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[24]  T. Kitamoto.  Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. , 2001, Journal of neurobiology.

[25]  M. Pankratz,et al.  Serotonergic pathways in the Drosophila larval enteric nervous system. , 2014, Journal of insect physiology.

[26]  H. Heinzel,et al.  The brain can eat: establishing the existence of a central pattern generator for feeding in third instar larvae of Drosophila virilis and Drosophila melanogaster. , 2010, Journal of insect physiology.

[27]  R. Stocker,et al.  Drosophila P[Gal4] lines reveal that motor neurons involved in feeding persist through metamorphosis. , 1998, Journal of neurobiology.

[28]  M. Pankratz,et al.  Suppression of food intake and growth by amino acids in Drosophila: the role of pumpless, a fat body expressed gene with homology to vertebrate glycine cleavage system. , 1999, Development.

[29]  A. Cohen.  Intersegmental coordinating system of the lamprey central pattern generator for locomotion , 1987, Journal of Comparative Physiology A.

[30]  F. Delcomyn.  Neural basis of rhythmic behavior in animals. , 1980, Science.

[31]  S. Grillner,et al.  On the central generation of locomotion in the low spinal cat , 1979, Experimental Brain Research.

[32]  U. Bässler,et al.  Pattern generation for stick insect walking movements—multisensory control of a locomotor program , 1998, Brain Research Reviews.

[33]  Barry J. Dickson,et al.  The Drosophila pheromone cVA activates a sexually dimorphic neural circuit , 2008, Nature.

[34]  Sreekanth H. Chalasani,et al.  Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators , 2009, Nature Methods.

[35]  S. W. Ranson,et al.  RESPONSES ELICITED BY STIMULATION OF THE MESENCEPHALIC TEGMENTUM IN THE CAT , 1930 .

[36]  Shawn R. Olsen,et al.  Cracking neural circuits in a tiny brain: new approaches for understanding the neural circuitry of Drosophila , 2008, Trends in Neurosciences.

[37]  H. Aberle,et al.  The expression pattern of the Drosophila vesicular glutamate transporter: a marker protein for motoneurons and glutamatergic centers in the brain. , 2006, Gene expression patterns : GEP.

[38]  S. Grillner,et al.  Neuronal network generating locomotor behavior in lamprey: circuitry, transmitters, membrane properties, and simulation. , 1991, Annual review of neuroscience.

[39]  E. Marder,et al.  Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. , 2007, Annual review of physiology.